Another Vapourer encounter

This sunny morning I had to stay at home, as my 7 year old daughter was unwell. On our trip to the doctor I noticed a flying insect I couldn't decide if it was butterfly or moth, it looked like it wanted to settle, so we waited until it did. If finally settled on some railings, flew again and resettled on another part of the railings, and then I realised it was a male Vapourer. This most wonderful of moths! Where there is a male Vapourer settling a female can't be far. Females don't look like moths, they are flightless, their wings reduced to little more than stumps, and they have bulging bodies full of eggs. Females actually move very little in their adult lives, as they just sit on top of their cocoon - which they made as a caterpillar and later emerged - waiting for males to home in their pheromones. Males are a wonderful chestnut colour, a bright moon-shaped white dot on each wing, with feathery antennae, and they fly often during the day.
The male had actually found a female on a corner of the railing and, almost immediately, they mated. I took a few photos with my phone and we carried on.
 On our way back a little later, we checked the railing. The male was gone, but the female wasn't wasting any time, and was busy laying eggs on the remains of her hairy cocoon.

Six-spot burnets: chemical weapons as nuptial gifts

Six-Spot Burnets, Zygaena filipendulae, are spectacular day flying moths. The contrast between their colour and the green meadows where they live makes them very obvious. Their body and forewing background are black, with a metallic green-blue sheen. Their forewings have six crimson-red spots. In addition they are large and heavy, and females like to perch conspicuously atop flower heads. You cannot miss a sitting burnet, but a flying one is even harder to miss: when they fly, a slow, buzzing, heavy flight, their crimson rear wings with a narrow black border become visible. As you could predict, this bright, black-with red spots contrasting colouration is a warning sign. Burnet moths are toxic, when they are injured, they release cyanide, a highly poisonous chemical. Cyanide compounds are found at some level in every life stage from egg to adult. The larvae sequester and store cyanogenic compounds from their food plants - Bird's Foot Trefoil, Lotus corniculatus - and all life stages are able to synthesize these chemicals themselves. However, production of the chemicals is costly, as larvae grow much more slowly when reared on varieties of Bird's Foot Trefoil lacking cyanogenic chemicals, as they have to synthesize them all themselves. There is a sudden loss of cyanogenic compounds from the last larval stage to the adult, and there also appears to be large variation in the amount of toxic chemicals in the adults. This could partly be explained by volatile hydrogen cyanide emissions by larvae - possibly as an antipredator strategy. Also, males convert some of their cyanogenic compounds into a pheromone; upon approaching a female, they release it. Females are able to determine how much pheromone a male is producing, the larger the quantity, the more likely the female is to accept him. But things get even more interesting. Mika Zagrobelny and co-workers, from the University of Copenhagen, collected Six-Spot Burnet larvae, pupa and adult from a local fallow field and made detailed measurements of the levels of cyanogenic compounds in the tissues of the different life stages, and also their toxic emissions. They found that females, as the larvae, emit hydrogen cyanide. Males are attracted to these chemical plumes, which form part of a pheromone cocktail produced by the female.

Average total cyanogenic compounds content in virgin and mated Z. filipendulae adults as well as in discarded males (which females would not mate with). Error bars are standard deviation. (figure modified from Zagrobelny et al. 2007).

The researchers then compared the cyanogenic compounds of virgin males and females, as well as mated males and females they paired up in the laboratory (see figure above). Virgin males and females had roughly similar levels of cyanogenic compounds. In contrast, after mating, females had larger levels, whereas males had lower levels. This indicates that during mating, males transfer some of these chemicals to the female, likely with the sperm. The levels of cyanogenic compounds in rejected males (males in an experimental pair that the females refused to mate with) were lower than average levels in virgin males, which suggests that females will mate preferentially with those males better loaded with chemical weapons. Why would the female benefit from acquiring more cyanide compounds. Possibly because the more she puts into eggs, the better defended they will be from predators, so this nuptial gift might be seen as a form of paternal behaviour. Alternatively, the female might gain through using this nuptial gift to produce more pheromone, attract further males and increase the vigour of her offspring.

A Six-Spot Burnet on Bird's Foot Trefoil

References
Zagrobelny M, Bak S, Olsen CE, & Møller BL (2007). Intimate roles for cyanogenic glucosides in the life cycle of Zygaena filipendulae (Lepidoptera, Zygaenidae). Insect biochemistry and molecular biology, 37 (11), 1189-97 PMID: 17916505

Racing male tree bumblebees

In the last two weeks, the garden has been overtaken by frenzied male bumblebees. They follow a set circuit, round and round, racing from bush to bush and then having a little bumble in each. If you wait for a bit on a particular spot on the route, you are likely to see another bumblebee a few minutes later passing by in the same direction, doing exactly the same. Most of the males I have been able to identify doing this are Bombus hypnorum. Today, a male B. hypnorum - which can be distinguished from the female by his white moustache - got trapped inside the conservatory and I had his portrait taken (above). Many male bumblebees have recently emerged from their nests, never to return, and their mission is to find queens and mate with as many as possible. In many bumblebee species, males' strategy consists on tracing a route, sometimes hundreds of meters long, often circular, depending on the species, and marking certain places along the route with pheromones produced by scent glands in their jaws. Males join already set routes and therefore many males, some of them probably their siblings, go round the same routes every day, stopping to feed occasionally. Queens encountering a route are attracted by the pheromone and are then intercepted by males. The discovery and first description of these male bumblebee flight paths - from Bombus hortorum males - dates back to Charles Darwin, from observations he carried out at Down House. Although he didn't realise pheromones were involved, he noticed bumblebee routes and them stopping and bumbling at places he called "buzzing places", and marveled at the fact that the same or very similar routes were used year after year:

I then followed their route for about a hundred and fifty yards until they came to a tall ash, and all along this line they buzzed at various fixed spots. At the far end, near a pollard oak, the track divided into two as shown in the plan. On some days all the bees flew in the direction I have described, but on others some arrived from the opposite direction. From observations made on favourable days, I think that the majority of individuals must fly in a wide circle. They stop every now and then to suck at flowers. I confirmed that whilst in flight they move at about ten miles an hour, but they lose a considerable amount of time at the buzzing places. The routes remain the same for a considerable time, and the buzzing places are fixed within an inch. I was able to prove this by stationing five or six of my children each close to a buzzing place, and telling the one farthest away to shout out " here is a bee " as soon as one was buzzing around. The others followed this up, so that the same cry of " here is a bee " was passed on from child to child without interruption until the bees reached the buzzing place where I myself was standing.

  This sketch of the grounds of Down House shows the part of the male bumblebee flight route studied by Darwin with the help of his children. What fun must have been to have him as a dad!

References

Freeman, R.B. (1968). Charles Darwin on the routes of male bumblebees. BULLETIN OF THE BRITISH MUSEUM (NATURAL HISTORY) HISTORICAL SERIES , 3 (6), 177-189.


Stiles, Edmund W. (1976). Comparison of Male Bumblebee Flight Paths: temperate and tropical. Journal of the Kansas Entomological Society., 49 (2), 266-274.

Dropping aphids and their alarm pheromones

Fortunately for the organic gardener, aphids have many predators: hoverfly larvae, lacewings, ladybirds, shield bugs and spiders eat them in numbers. Although aphids appear defenceless against their predators, they have evolved a suite of antipredator responses. Some aphids have warning coloration and sequester chemicals from their feeding plants that are distasteful or toxic to their predators, other release toxic chemicals or waxes and a few have a hard-skinned soldier caste to defend the colony, yet others maintain an army of ants that defend them. The most common form of defence - both against predators or parasitoids - is however, behavioural: the aphids move away or drop from the leaf they are feeding on when they sense an approaching predator.
 Dropping is very effective in reducing immediate risk: aphids fall away from the approaching danger onto the ground. Once there other costs become apparent: the aphid may be far from the host plant and is exposed to ground predators or to desiccation.
 The orange tree in my conservatory is infested with aphids. I took advantage of the abundance of 7 spot ladybirds in the garden and brought a few onto the tree, placing them on particularly infested branches. I was pleasantly surprised by the eagerness with which the ladybirds took to the intended job. They started munching aphids straight away, clearing whole shoots in a few minutes. After a little observation, however, it became apparent that it was the aphid's behaviour which was mostly responsible for the shoots being cleared. The undisturbed aphids sat motionless, on a living carpet feeding on the tender leaf sap nearby. In contrast, as soon as a ladybird attacked, the aphids on the same leaf came alive and some started to move away, going into another leaf, while many aphids dropped to the ground as the ladybird fed on their unfortunate siblings. The following two photos illustrate this. They were taken about 27 seconds apart. In the first one, notice the three aphids on the tip of the leaf. In the second photo, these aphids have dropped to the ground, leaving just a couple of aphid molts stuck to the leaf tip, while the ladybird is still feeding on an aphid, motionless.

 Ladybirds are very effective at eliciting the drop response from aphids, especially when compared to smaller, less energetic feeders, as demonstrated in experiments by John Losey and Robert Denno on pea aphids feeding on alfalfa exposed to a predator insect.

This means that on average 60% of aphids feeding on a plant stem dropped to the ground when a 7 spot ladybird (Coccinella septempunctata) was introduced, in sharp contrast to the lower dropping response to the bugs and the control. Given the higher mortality of aphids on the ground, it follows that ladybirds would be very effective clearing aphid infestations through direct predation, and their indirect effect on aphids dropping from the plant.
 What mechanisms are responsible for this dropping behaviour? or, put differently, how do aphids sense that a predator is approaching? Dropping behaviour happens in response to predator contact, vibrations generated by the predator, or in response to an alarm pheromone secreted by individual aphids when attacked. This chemical signal, (E)-ß-farnesene (EBF), is secreted in dropplets by the cornicles, little tubes at the rear of the aphid, and they may impregnate the predator, which in its next move will elicit the dropping response before actually attacking another aphid.
 The release of an alarm pheromone by an individual that is likely to be eaten by a predator seems paradoxical. What benefit can this individual gain from its production? An alarm pheromone can be adaptive when the benefit is shared by relatives. This is indeed the case in aphids: groups of aphids feeding in close contact are likely to be members of the same clone, that is, they are genetically identical, as aphids often reproduce parthenogenetically. The alarm pheromone also has longer lasting effects benefiting the individual relatives, as the aphids that have been exposed to the chemical tend to produce winged offspring, which will likely disperse away from predators, in the case of the ladybird attacker, they will be likely to avoid the following generation of ladybird larvae.

References
LOSEY, J., & DENNO, R. (1998). The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour. Ecological Entomology, 23 (1), 53-61 DOI: 10.1046/j.1365-2311.1998.00102.x
Schwartzberg, E., Kunert, G., Stephan, C., David, A., Röse, U., Gershenzon, J., Boland, W. & Weisser, W. (2007). Real-Time Analysis of Alarm Pheromone Emission by the Pea Aphid (Acyrthosiphon pisum) Under Predation. Journal of Chemical Ecology, 34 (1), 76-81 DOI: 10.1007/s10886-007-9397-8